Female mouse fetal loss mediated by maternal autoantibody

Journal of Experimental Medicine

Volumn 209, Issue 6, 2012, Pages 1083-1089

  Wang, Li ^a   Zhou, Dun ^a   Lee, Ji ^b   Niu, Haitao ^a   Faust, Thomas W ^a   Frattini, Stephen ^a   Kowal, Czeslawa ^a   Huerta, Patricio T ^a   Volpe, Bruce T ^a   Diamond, Betty ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; MATERNAL ANTIBODY; MATERNAL AUTOANTIBODY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN STEM; CONTROLLED STUDY; CROSS REACTION; FEMALE; FETAL WELL BEING; FETUS DEVELOPMENT; FETUS WASTAGE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SEX RATIO; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, ANTINUCLEAR; APOPTOSIS; AUTOANTIBODIES; BRAIN; FEMALE; FETAL DEATH; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED BALB C; NEURONS; OLIGOPEPTIDES; PREGNANCY; RECEPTORS, N-METHYL-D-ASPARTATE; SEX FACTORS; SEX RATIO;

EID: 84863458065     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111986     Document Type: Article

References (26)

1. Chen, X., R. Watkins, E. Delot, R. Reliene, R.H. Schiestl, P.S. Burgoyne, and A.P. Arnold. 2008. Sex difference in neural tube defects in p53-null mice is caused by differences in the complement of X not Y genes. Dev. Neurobiol. 68:265-273. http://dx.doi.org/10.1002/dneu.20581
2. Cyr, M., C. Thibault, M. Morissette, M. Landry, and T. Di Paolo. 2001. Estrogen-like activity of tamoxifen and raloxifene on NMDA receptor binding and expression of its subunits in rat brain. Neuropsychopharmacology. 25:242-257. http://dx.doi.org/10.1016/S0893-133X(01)00233-0
3. DeGiorgio, L.A., K.N. Konstantinov, S.C. Lee, J.A. Hardin, B.T. Volpe, and B. Diamond. 2001. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 7:1189-1193. http://dx.doi.org/10.1038/nm1101-1189
4. Faust, T.W., E.H. Chang, C. Kowal, R. Berlin, I.G. Gazaryan, E. Bertini, J. Zhang, J. Sanchez-Guerrero, H.E. Fragoso-Loyo, B.T. Volpe, et al. 2010. Neurotoxic lupus autoantibodies alter brain function through two distinct mechanisms. Proc. Natl. Acad. Sci. USA. 107:18569-18574. http://dx.doi.org/10.1073/pnas.1006980107
5. Hardingham, G.E., and H. Bading. 2010. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11:682-696. http://dx.doi.org/10.1038/nrn2911
6. Hsu, C., Y.L. Hsieh, S.I. Lue, and H.K. Hsu. 1999. Sex-specific expression of N-methyl D-aspartate receptor (NMDAR) in the preoptic area of neonatal rats. Neurosci. Lett. 262:85-88. http://dx.doi.org/10.1016/S0304-3940(99)00038-5
7. Iijima, T., H. Tada, Y. Hidaka, N. Mitsuda, Y. Murata, and N. Amino. 1997. Effects of autoantibodies on the course of pregnancy and fetal growth. Obstet. Gynecol. 90:364-369. http://dx.doi.org/10.1016/S0029-7844(97)00283-4
8. James, W.H. 2007. The sex ratio of offspring of patients with systemic lupus erythematosus. Lupus. 16:65-66. http://dx.doi.org/10.1177/0961203306073365
9. Khalil, M., K. Inaba, R. Steinman, J. Ravetch, and B. Diamond. 2001. T cell studies in a peptide-induced model of systemic lupus erythematosus. J. Immunol. 166:1667-1674.
10. Koopman, P., A. Münsterberg, B. Capel, N. Vivian, and R. Lovell-Badge. 1990. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature. 348:450-452. http://dx.doi.org/10.1038/348450a0
11. Kowal, C., L.A. Degiorgio, J.Y. Lee, M.A. Edgar, P.T. Huerta, B.T. Volpe, and B. Diamond. 2006. Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc. Natl. Acad. Sci. USA. 103:19854-19859. http://dx.doi.org/10.1073/pnas.0608397104
12. Lee, J.Y., P.T. Huerta, J. Zhang, C. Kowal, E. Bertini, B.T. Volpe, and B. Diamond. 2009. Neurotoxic autoantibodies mediate congenital cortical impairment of offspring in maternal lupus. Nat. Med. 15:91-96. http://dx.doi.org/10.1038/nm.1892
13. Liu, Y., T.P. Wong, M. Aarts, A. Rooyakkers, L. Liu, T.W. Lai, D.C. Wu, J. Lu, M. Tymianski, A.M. Craig, and Y.T. Wang. 2007. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 27:2846-2857. http://dx.doi.org/10.1523/JNEUROSCI.0116-07.2007
14. Matturri, L., I. Minoli, A.M. Lavezzi, A. Cappellini, S. Ramos, and L. Rossi. 2002. Hypoplasia of medullary arcuate nucleus in unexpected late fetal death (stillborn infants): a pathologic study. Pediatrics. 109:E43. http://dx.doi.org/10.1542/peds.109.3.e43
15. Meyer, U., J. Feldon, and S.H. Fatemi. 2009. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33:1061-1079. http://dx.doi.org/10.1016/j.neubiorev.2009.05.001
16. Monyer, H., R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P.H. Seeburg. 1992. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science. 256:1217-1221. http://dx.doi.org/10.1126/science.256.5060.1217
17. Morel, L., X.H. Tian, B.P. Croker, and E.K. Wakeland. 1999. Epistatic modifiers of autoimmunity in a murine model of lupus nephritis. Immunity. 11:131-139. http://dx.doi.org/10.1016/S1074-7613(00) 80088-6
18. Novack, V., O. Erez, L. Novack, A. Jotkowitz, A. Meir, and M. Mazor. 2006. Sex distribution of newborns to mothers with systemic lupus erythematosus. Epidemiology. 17:341-342. http://dx.doi.org/10.1097/01.ede.0000209417.14819.44
19. Oster, E. 2005. Hepatitis B and the case of the missing women. J. Polit. Econ. 113:1163-1216. http://dx.doi.org/10.1086/498588
20. Portera-Cailliau, C., D.L. Price, and L.J. Martin. 1996. N-methyl-D-aspartate receptor proteins NR2A and NR2B are differentially distributed in the developing rat central nervous system as revealed by subunit-specific antibodies. J. Neurochem. 66:692-700. http://dx.doi.org/10.1046/j.1471-4159.1996.66020692.x
21. Putterman, C., and B. Diamond. 1998. Immunization with a peptide surrogate for double-stranded DNA (dsDNA) induces autoantibody production and renal immunoglobulin deposition. J. Exp. Med. 188:29-38. http://dx.doi.org/10.1084/jem.188.1.29
22. Salmon, J.E., G. Girardi, and M.D. Lockshin. 2007. The antiphospholipid syndrome as a disorder initiated by inflammation: implications for the therapy of pregnant patients. Nat. Clin. Pract. Rheumatol. 3:140-147, quiz:1: 187. http://dx.doi.org/10.1038/ncprheum0432
23. Sen, A. 1992. Missing women. BMJ. 304:587-588. http://dx.doi.org/10.1136/bmj.304.6827.587
24. Shi, L., N. Tu, and P.H. Patterson. 2005. Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus. Int. J. Dev. Neurosci. 23:299-305. http://dx.doi.org/10.1016/j.ijdevneu.2004.05.005
25. von Engelhardt, J., I. Coserea, V. Pawlak, E.C. Fuchs, G. Köhr, P.H. Seeburg, and H. Monyer. 2007. Excitotoxicity in vitro by NR2A- and NR2B-containing NMDA receptors. Neuropharmacology. 53:10-17. http://dx.doi.org/10.1016/j.neuropharm.2007.04.015
26. Woolley, C.S., N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin. 1997. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci. 17:1848-1859.